Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment

Abstract

Phytoplankton is a key component of aquatic microbial communities, and metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon (DOC). Yet, the impact of primary production on bacterial activity and community composition remains largely unknown, as, for example, in the case of aerobic anoxygenic phototrophic (AAP) bacteria that utilize both phytoplankton-derived DOC and light as energy sources. Here, we studied how reduction of primary production in a natural freshwater community affects the bacterial community composition and its activity, focusing primarily on AAP bacteria. The bacterial respiration rate was the lowest when photosynthesis was reduced by direct inhibition of photosystem II and the highest in ambient light condition with no photosynthesis inhibition, suggesting that it was limited by carbon availability. However, bacterial assimilation rates of leucine and glucose were unaffected, indicating that increased bacterial growth efficiency (e.g., due to photoheterotrophy) can help to maintain overall bacterial production when low primary production limits DOC availability. Bacterial community composition was tightly linked to light intensity, mainly due to the increased relative abundance of light-dependent AAP bacteria. This notion shows that changes in bacterial community composition are not necessarily reflected by changes in bacterial production or growth and vice versa. Moreover, we demonstrated for the first time that light can directly affect bacterial community composition, a topic which has been neglected in studies of phytoplankton-bacteria interactions. IMPORTANCE Metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon in aquatic environments, and yet how changes in the rate of primary production affect the bacterial activity and community composition remains understudied. Here, we experimentally limited the rate of primary production either by lowering light intensity or by adding a photosynthesis inhibitor. The induced decrease had a greater influence on bacterial respiration than on bacterial production and growth rate, especially at an optimal light intensity. This suggests that changes in primary production drive bacterial activity, but the effect on carbon flow may be mitigated by increased bacterial growth efficiencies, especially of light-dependent AAP bacteria. Bacterial activities were independent of changes in bacterial community composition, which were driven by light availability and AAP bacteria. This direct effect of light on composition of bacterial communities has not been documented previously.

The Prokaryotic Microbiome of Acropora digitifera is Stable under Short-Term Artificial Light Pollution

“…Members of the AAPB family can also utilize various organic and inorganic compounds, perform sulfur oxidation, carbon monoxide oxidation, and produce secondary metabolites [ 60 ]. Light directly affects and stimulates the growth rates and abundance of natural populations of marine AAPB, which explains their abundance in the corals experiencing light pollution at night [ 61 , 62 ]. Anoxygenic phototrophs have previously been detected in the skeletons of the scleractinian corals Montipora monasteriata , Porites cylindrica, and Isopora palifera [ 63 , 64 ].…”

Infection with intracellular parasite Amoeboaphelidium protococcarum induces shifts in associated bacterial communities in microalgae cultures

“…The microenvironment of the phycosphere allows the exchange of manifold metabolites and chemical compounds that can result in a wide spectrum of mutualistic, commensalistic, antagonistic, competitive, or parasitic relationships (Kazamia et al 2016;Ramanan et al 2016;Seymour et al 2017;Cirri and Pohnert 2019). Such algae-bacterial relationships can be altered by abiotic factors like temperature and/or light availability (Mayers et al 2016;Piwosz et al 2020). The relationship of algae and associated bacterial communities has to be therefore considered as a dynamic range of subsequent states of highly complex networks influenced by changing environmental conditions (Gurung et al 1999;Seyedsayamdost et al 2014;Fuentes et al 2016;Mayers et al 2016;Cirri and Pohnert 2019).…”

Diversity of Aerobic Anoxygenic Phototrophs and Rhodopsin-Containing Bacteria in the Surface Microlayer, Water Column and Epilithic Biofilms of Lake Baikal

“…The taxonomic composition of AAP communities in Lake Baikal is similar to that in other freshwater bodies [ 14 , 15 , 16 , 18 , 22 , 88 , 89 ]. As in Lake Baikal, Rhodobacterales and Burkholderiales dominated, and Rhizobiales, Rhodospirillales, and Sphingomonadales were detected almost in every studied water body.…”

“…Recently, the photosynthesis genes pufLM and bchY from the Limnohabitans representatives were detected [ 21 ]. Now it is known that Limnohabitans comprises a big part of the AAP community in freshwater ecosystems [ 21 , 89 ]. A considerable amount (1.8%) of our 16S rRNA sequences was identified as Limnohabitans .…”